ORIGINAL RESEARCHINTERVENTIONAL

Long-Term Outcomes of Patients with Stent Tips Embeddedinto Internal Carotid Artery Branches during Aneurysm Coiling

X S.P. Ban, X O.-K. Kwon, X S.U. Lee, X J.S. Bang, X C.W. Oh, X H.J. Jeong, X M.J. Cho, X E.-A. Jeong, and X T. Kim

ABSTRACT

BACKGROUND AND PURPOSE: During stent-assisted coiling of ICA aneurysms, stent tips are sometimes unintentionally embedded intoICA branches. Stent tips can be visualized because they have radiopaque markers. Concerns regarding stent tip misplacement include risksof artery perforation and occlusion. The aim of this study was to evaluate the long-term outcomes of ICA branches with embedded stenttips.

MATERIALS AND METHODS: ICA branches with embedded stent tips were identified among 35 patients with unruptured ICA aneurysmstreated with stent-assisted coiling between November 2003 and November 2014. Patient clinical and angiographic outcomes associatedwith the embedded stent tip were analyzed.

RESULTS: Most of the 35 studied aneurysms were paraclinoid ICA aneurysms (n � 30). The most commonly involved ICA branch was theposterior communicating artery (26 patients, 74.3%), followed by the anterior choroidal artery (8 patients, 22.9%) and ophthalmic artery (1patient, 2.9%). During the follow-up period (38.6 � 17.9 months), no new neurologic deficits developed. Neither hemorrhagic nor throm-boembolic events occurred. Angiography was performed during the final follow-up evaluation at a mean of 32.7 � 18.0 months, and all ICAbranches with embedded stent tips showed patent blood flow without severe luminal narrowing.

CONCLUSIONS: In our experience, placement of a stent tip into ICA branches during stent-assisted coiling was not associated with anymajor adverse events.

ABBREVIATIONS: AchoA � anterior choroidal artery; OphA � ophthalmic artery; PcomA � posterior communicating artery; SAC � stent-assisted coiling

Self-expandable stents have provided considerable assis-

tance in increasing the indications for aneurysm coiling.

Complex and wide-neck aneurysms, which are considered

challenging or impossible to treat with simple coiling, can now

be treated.1

Generally, self-expandable stents for cerebral aneurysm

treatment have proximal and distal radiopaque markers to

identify the end of the stent. These markers are made from

coiled tantalum wire or platinum bands, which are larger than

the stent strut itself. The markers are attached to the triangular

pointed stent tip wire (strut) part. During stent-assisted coil-

ing (SAC), the stent tip can sometimes be unintentionally em-

bedded into a small arterial branch. We have occasionally en-

countered this event, particularly during SAC performed for

ICA aneurysms, which is well-visualized due to the radiopaque

markers. This phenomenon raises concerns regarding the po-

tential risks of arterial perforation due to the sharp end and

constant arterial pulsating motion of the stent, as well as the

chances of vessel occlusion. Stent tip markers may also disrupt

blood flow by themselves or by intimal injury (thrombus for-

mation or intimal hyperplasia), which may then lead to infarc-

tion. Despite these concerns, we were unable to find a report

regarding the clinical or radiologic outcomes of embedded

stent tips within ICA branches. Thus, we reviewed our series of

patients who had undergone SAC for unruptured ICA aneu-

rysms and in whom stent tips were embedded within the ICA

branch orifice. We analyzed clinical and angiographic data to

identify the outcomes of these cases.

MATERIALS AND METHODSPatientsThis study was approved by the institutional review board at our

institution. Informed consent from enrolled patients was waived.

Received November 7, 2017; accepted after revision January 3, 2018.

From the Department of Neurosurgery, Seoul National University Bundang Hospi-tal, Seongnam, Gyeonggi-do, Korea.

Please address correspondence to Tackeun Kim, MD, Department of Neurosur-gery, Seoul National University Bundang Hospital, 82 Gumi-ro 173 beon-gil, Bun-dang-gu, Seongnam-si, Gyeonggi-do, 13620, Korea; e-mail: midabo@naver.com

Indicates article with supplemental on-line table.

http://dx.doi.org/10.3174/ajnr.A5583

864 Ban May 2018 www.ajnr.org

We retrospectively reviewed patient medical records, including

pre- and posttreatment radiologic studies. Our data base con-

tained a series of 2730 patients with 2998 intracranial aneurysms

treated with endovascular techniques between November 2003

and November 2014. Among these patients, 886 with 947 unrup-

tured intracranial aneurysms were treated with SAC. In this series,

data from 664 patients with 706 ICA aneurysms who were treated

with SAC were collected and reviewed. Among these patients, the

placement of a stent tip into an ICA branch was identified in 36

aneurysms of 36 patients. In our subsequent analysis, 1 patient

who was lost to follow-up was excluded. The patient selection

criteria are outlined in Fig 1.

Antiplatelet Therapy Protocol and EndovascularProceduresPatients with unruptured aneurysms received dual antiplatelet

agents (100 mg of aspirin and 75 mg of clopidogrel) for at least 5

days before embolization. One day before coil embolization,

P2Y12 reaction units were measured using VerifyNow (Accumet-

rics, San Diego, California). Patients with clopidogrel resistance

(�220 P2Y12 reaction units) received a modified antiplatelet reg-

imen. Details regarding our antiplatelet agent protocol have been

previously described.2 A 3000-IU bolus dose of intravenous hep-

arin was administered after the placement of the femoral artery

sheath, and heparin was later infused at an hourly booster dose of

1000 IU, with monitoring of the activated clotting time. After the

procedure, dual antiplatelet treatment continued for 1 year; after

1 year, this therapy was exchanged for daily oral treatment with

100 mg of aspirin for an additional year.

All endovascular procedures were performed with the patient

under general anesthesia using an Integris Allura scanner (Philips

Healthcare, Best, the Netherlands) before 2014 and an IFNX-

8000V scanner (Toshiba, Tokyo, Japan) from 2014. The jailing

technique was mainly used for SAC. First, a target aneurysm was

selected using a microcatheter (Excelsior SL-10; Stryker Neuro-

vascular, Kalamazoo, Michigan). Then, the parent artery was nav-

igated with another microcatheter (Prowler Select Plus, Codman

& Shurtleff, Raynham, Massachusetts; or Neuro Renegade,

Stryker Neurovascular) for stent delivery. A stent was deployed

into the parent artery across the aneurysm neck. Then, the aneu-

rysm was coiled using platinum detachable coils until complete

occlusion was achieved or further coiling was deemed unsafe.

Stent type, length, and placement were determined by the neuro-

vascular team and were based on aneurysm location and neck

diameter. Among 706 ICA aneurysms treated with SAC, Enter-

prise stents (Codman & Shurtleff) were most commonly used

(n � 607, 86.0%), followed by Neuroform stents (Stryker Neuro-

vascular) in 71 cases (10.1%). The other stents used included

Low-Profile Visualized Intraluminal Support stents (MicroVention,

Tustin, California) in 19 cases (2.7%) and Solitaire AB stents

(Covidien, Irvine, California) in 9 cases (1.3%). Of the 35

cases, 32 were treated with a single Enterprise stent and 3 were

treated with a single Neuroform stent.

Stent Tips of Enterprise and Neuroform StentsThe Enterprise stent is a laser-cut stent with a closed-cell design.

This stent has flared proximal and distal ends, consisting of 4

pointed parts. Each end has 4 radiopaque tantalum coil markers

for increased visibility, which flare out for fixation of the stent

onto the vascular wall when fully deployed (Fig 2A). Due to the

sharp, pointed, flaring parts, these stents can be embedded into

the small ICA branches. The radiopaque markers of the tips allow

them to be clearly visualized. The diameter of a radiopaque

marker was thicker than that of the stent strut. Stent strut

width and thickness were approximately 0.0015 inches (0.0381

mm) and 0.0031 inches (0.0787 mm), respectively. The thick-

ness and length of the radiopaque marker were approximately

0.008 inches (0.2032 mm) and 0.043 inches (1.0922 mm), re-

spectively (Fig 2B, -C).

The Neuroform stent is a laser-cut stent with an open-cell or

half-open-cell design. This stent has 4 distal and 4 proximal ra-

diopaque platinum markers (Fig 2D). Each open-cell segment

may serve as a separate fixing device to enhance the apposition of

the stent to the vessel wall like the flared ends of the Enterprise

stent. Like the Enterprise stent, the stent tip may be placed and

embedded into the branch orifice. Stent strut width and thickness

were approximately 0.0027 inches (0.0686 mm). The thickness

and length of the radiopaque marker were approximately 0.0116

inches (0.2946 mm) and 0.030 inches (0.762 mm), respectively

(Fig 2E, -F).

Evaluation of Clinical and Radiologic OutcomesThe clinical outcomes of all patients were evaluated using the mRS

score on admission and at the final outpatient follow-up visit.

FIG 1. Outline of patient selection.

AJNR Am J Neuroradiol 39:864 – 68 May 2018 www.ajnr.org 865

Newly developed neurologic deficits as well as hemorrhagic and

thromboembolic complications during follow-up periods were

also reviewed. The placement and embedding of a stent tip with a

marker into a branching artery was defined as a stent tip that was

placed at the level of branching arteries, with the tip marker clearly

visualized within the artery orifice via angiographic views, in-

cluding rotational angiograms. According to our institutional

protocol, patients underwent imaging follow-up at 3, 6, 12, 24,

and 36 months with skull plain radiography and at 1, 2, and 3

years with 3D-TOF MRA, including source imaging. Any time

a major recanalization was found, DSA was performed. DSA

follow-up studies were routinely conducted between 3 and 5

years after coil embolization if no major recanalization of an

aneurysm was suspected. In this study, each patient underwent

a minimum of 12 months of radiologic follow-up. Vessel pa-

tency was documented by follow-up DSA. If follow-up DSA

was not performed, vessel patency was confirmed using the

follow-up axial MRA source images.

Data AnalysisAll statistical analyses were performed using SPSS software

(Version 22.0; IBM, Armonk, New York). Continuous vari-

ables are presented as mean � SD. Binary variables were com-

pared using the Fisher exact test. Statistical significance was set

at P � .05.

RESULTSThe overview of patients with stent tips embedded into the ICA

branches is summarized in the On-line Table. Eight (22.9%) pa-

tients were men, and 27 (77.1%) were women. The mean age was

49.3 � 12.8 years (range, 21–76 years). The cases included 30

(85.7%) paraclinoid ICA aneurysms, 3 (8.6%) ophthalmic artery

(OphA) aneurysms, 1 (2.9%) cavernous ICA aneurysm, and 1

(2.9%) posterior communicating artery (PcomA) aneurysm. The

most common ICA branching artery with an embedded stent tip

was the PcomA (26 patients, 74.3%).

Other involved branching arteries in-

cluded the anterior choroidal artery(AchoA) in 8 (22.9%) patients and theOphA in 1 (2.9%) patient. The incidenceof stent tips embedded within ICAbranches was not associated with thetype of stent (closed-cell-design stent,5.3%, versus open-cell-design stent,

4.2%; P � .424). Most of these events

occurred during deployment of the dis-

tal end of the stent at the upward ICA

curvature near the ICA branches (32

cases, 91.4%), followed by unintentional

stent advancement during microcath-

eter manipulation (3 cases, 8.6%).The mean clinical follow-up dura-

tion was 38.6 � 17.9 months (range,

12–91 months). The preoperative mRS

score was 0 in 30 (85.7%) patients and 1

in 5 (14.3%) patients. The final fol-

low-up mRS score was 0 in 32 (91.4%)

patients and 1 in 3 (8.6%) patients. No

patient experienced mRS score deterioration. No newly devel-

oped neurologic deficits were observed. Neither hemorrhagic nor

thromboembolic (or ischemic) complications occurred during

the follow-up period.

The mean angiographic follow-up duration was 32.7 � 18.0

months (range, 12–91 months). The mean initial diameter of the

ICA branches with embedded stent tips was 1.79 � 0.69 mm

(range, 0.51–2.81 mm). On final follow-up angiography (15

cases were measured by MRA with source imaging and 20 cases

were measured by DSA), all ICA branches with an embedded

stent tip had persistent blood flow without severe luminal nar-

rowing. In 1 case, the radiopaque stent marker appeared to

penetrate the PcomA. In the angiogram, the marker appeared

to be located outside the arterial wall. However, no clinical

event was observed (case 11).

Illustrative Cases

Case 11. A 64-year-old patient presented with an unruptured left

paraclinoid ICA aneurysm (Fig 3A, -B). The aneurysm was treated

with coil embolization using a 4.5 � 20 mm Neuroform stent.

Postembolization angiography showed the placement of the stent

marker in the PcomA (Fig 3C, -D). Although a radiopaque stent

marker appeared to penetrate the PcomA in the 5-year-follow-up

angiograms, the PcomA was patent and no hemorrhagic compli-

cation occurred (Fig 3E, -F).

Case 13. A 23-year-old patient presented with an unruptured left

paraclinoid ICA aneurysm (Fig 4A, -B). The aneurysm was treated

with coil embolization using a 4.5 � 22 mm Enterprise stent.

Postembolization angiography showed the placement of the stent

marker into the AchoA (Fig 4C, -D). Follow-up angiography at 3

years showed patent blood flow to the AchoA without severe lu-

minal narrowing (Fig 4E, -F).

FIG 2. A, Flared ends of the Enterprise stent. B, Length of the flare marker of the Enterprise stent.C, Width of the flare marker and stent strut of the Enterprise stent. D, End of the Neuroformstent. E, Length of the platinum marker of the Neuroform stent. F, Width of the platinum markerand stent strut of the Neuroform stent. Asterisk indicates 0.1 mm.

866 Ban May 2018 www.ajnr.org

DISCUSSIONThis study demonstrates that stent tip embedding into the

ICA branches during SAC of cerebral aneurysms was not asso-

ciated with any major adverse events. No arterial rupture or

occlusion was observed during at least 1 year (12–91 months)

of follow-up.

During SAC of ICA aneurysms, stent tips can be deployed and

unintentionally embedded into ICA branching arteries due to

their characteristics. In our study, the incidence of this event was

5.1%, and the PcomA was the most commonly involved ICA

branch, followed by the AchoA. Although we attempted to deploy

stents so as avoid embedding the stent tip into the orifice of these

ICA branches, the distal part of a stent

may be deployed flat around the PcomA

and AchoA due to the ICA curvature,

resulting in stent tips embedding into

these ICA branches. In this study, this

issue was the most common cause

of an embedded stent tip within ICA

branches (91.4%). Because the ICA usu-

ally starts to curve upward near the

PcomA and the diameter of the PcomA

is commonly larger than that of the

AchoA, it is likely that the stent tips are

more easily embedded into the PcomA

than into the AchoA.

Regarding the structure of the stents,

because a closed-cell-design stent im-

mediately transmits a force from one

end to the other end, embedding of a

stent tip into ICA branches due to

stent advancement during microcath-

eter manipulation may be more com-

monly observed in patients receiving

a closed-cell-design stent. Concerning

this possible mechanism, in this study,

all 3 cases (8.6%) in which the distal part

of a stent was initially deployed proxi-

mally near the PcomA and then ad-

vanced and embedded into the PcomA

due to microcatheter manipulation were

treated with the Enterprise stent (closed-

cell design). However, because the most

common cause of embedding of a stent

tip into ICA branches was the ICA cur-

vature, no association was observed

among the types of stents used in this

study.

This event raises the following con-

cerns: vessel rupture (perforation) and

occlusion. Vessel rupture due to the

forceful advancement of stents has been

reported. The sharp ends of the stent

may contribute to arterial rupture.3,4

The lack of this complication in our

study suggests that stent ends were in-

serted into the branching arteries with-

out excessive force. The presence of an

embedded stent tip in small arteries can be a risk factor for further

arterial injury with persistent arterial pulsation, at least theoreti-

cally. However, this study shows that this risk is not likely in

practice.

Vessel occlusion or significant flow disruption may develop

through intimal injury by the stent tip in a delayed manner as well

as mechanical occlusion by stent tips and large markers them-

selves during the acute period. Therefore, we can consider several

plausible mechanisms of vessel occlusion or flow disruption. A

stent covering the small arterial ostium does not usually lead to

arterial occlusion.5-7 Unlike a simple stent covering the arterial

FIG 3. A, An unruptured left paraclinoid ICA aneurysm on pre-embolization DSA. B, 3D image ofthe aneurysm. C and D, A distal stent marker of the Neuroform stent (arrow) is deployed into theposterior communicating artery, as shown on postembolization angiography. E and F, The bloodflow to the PcomA with malposition of the stent marker is patent on 5-year-follow-up cerebralangiography. A radiopaque stent marker appears to penetrate the PcomA (arrow).

FIG 4. A left paraclinoid ICA aneurysm is shown on pre-embolization DSA (A) and 3D imaging (B).C and D, Postembolization angiography shows the malposition of the Enterprise stent marker inthe anterior choroidal artery (arrow). E and F, Follow-up cerebral angiography at 3 years showspersistent blood flow to the AchoA.

AJNR Am J Neuroradiol 39:864 – 68 May 2018 www.ajnr.org 867

orifice, embedded stent tips have greater luminal occupancy due

to the sharp triangular stent tip labeled with a radiopaque marker.

Radiopaque markers at the stent tip have a larger area and volume

than the stent. In a coronary artery study of a swine model, 2-fold

thicker stents were 49% more thrombogenic and increased flow

stagnation and disruption.8 Stent markers are 5.3-fold thicker

than the stent strut in the Enterprise stent and 4.3-fold thicker

than the stent strut in the Neuroform stent. In addition, persistent

arterial pulsation with stent tips at the arterial orifice may also lead

to further repeat intimal injury and subsequent thrombus forma-

tion and neointimal hyperplasia.4,9 However, this issue was not

detected in our series of patients. The triangular shape of the stent

tip may reduce such risks by stopping further advancement of the

stent strut into the arterial lumen. The persistent need for blood

flow to the ICA branches may also help prevent occlusion or se-

vere stenosis.10

Furthermore, luminal narrowing by intimal hyperplasia may

be spontaneously reversed.11 The proliferated neointima reaches

a maximal thickness by 2 months, and this neointimal layer grad-

ually becomes thin, more sclerotic, and less cellular by 8 months.

Kim et al9 reported that most in-stent stenoses would spontane-

ously improve to 91% of the initial mean diameter after 24

months. In our series, we did not perform angiographic follow-up

until 12 months after SAC. Thus, luminal narrowing before this

time was not confirmed. However, neither ischemic symptoms

nor infarction developed in our study. One case (case 11) showed

a radiopaque stent marker that appeared to be outside the PcomA

lumen on 5-year-follow-up angiographic images. It is uncertain

whether the stent tip was located outside the artery. However, no

clinical symptoms or radiologic findings associated with arterial

rupture were observed immediately after coiling, which suggests

that the marker was more likely inside the artery and encased by

neointimal hyperplasia. Although the mechanism has not yet

been clearly determined, this study demonstrates that vessel oc-

clusion by an embedded stent tip into the lumen is not common

in practice.

Our study has several limitations including its retrospective

nature and small sample size from a single institution. Further-

more, this study showed only the results of placement of stent

markers from Enterprise and Neuroform stents, which are only 2

varieties among many expandable stents. In 15 cases, follow-up

imaging was performed with TOF-MRA according to our institu-

tional protocol. Although the patency of ICA branches with em-

bedded stent tips was confirmed by MRA images, we did not show

the changes in the diameters of ICA branches with embedded

stent tips because this would be inaccurate due to the metal arti-

facts of the embedded stent tip on MRA images. Further research

using computational fluid dynamics is warranted to more com-

pletely understand the changes in the diameter of ICA branches

with embedded stent tips and the difference in the flow distur-

bance effect between stent struts and radiopaque markers.

CONCLUSIONSIn our experience, placement of a stent tip into ICA branches

during SAC was not associated with any major adverse events.

During 12–91 months of follow-up, vessel rupture, significant

blood flow reduction, and arterial occlusion were not detected.

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